Co-expression of GAP-43 and nNOS in avulsed motoneurons and their potential role for motoneuron regeneration

Nitric Oxide - Biology and Chemistry

Volumn 23, Issue 4, 2010, Pages 258-263

  Yuan, Qiuju ^a,c   Hu, Bing ^a   Chu, Tak Ho ^a   Su, Huanxing ^a   Zhang, Wenming ^a   So, Kwok Fai ^a,b,d   Lin, Zhixiu ^c   Wu, Wutian ^a,b,d  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d JINAN UNIVERSITY   (China)

Author keywords

Axonal injury; Motoneuron; Nitric oxide synthase; Regeneration; Spinal cord

Indexed keywords

NEUROMODULIN; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ARTICLE; AXONAL INJURY; FEMALE; IMMUNOHISTOCHEMISTRY; MOTONEURON; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL ROOT; SPINE INJURY;

RATTUS;

EID: 77958153558     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2010.07.006     Document Type: Article

References (50)

1. Dawson V.L. Nitric oxide: role in neurotoxicity. Clin. Exp. Pharmacol. Physiol. 1995, 22:305-308.
2. Vajragupta O., Boonyarat C., Murakami Y., Tohda M., Musatmoto K., Olson A.J., Watanabe H. A novel neuroprotective agent with antioxidant and nitric oxide synthase inhibitory action. Free Radic. Res. 2006, 40:685-695.
3. Goyagi T., Goto S., Bhardwaj A., Dawson V.L., Hurn P.D., Kirsch J.R. Neuroprotective effect of sigma(1)-receptor ligand 4-phenyl-1-(4-phenylbutyl) piperidine (PPBP) is linked to reduced neuronal nitric oxide production. Stroke 2001, 32:1613-1620.
4. Li W., Lee N.T., Fu H., Kan K.K., Pang Y., Li M., Tsim K.W., Li X., Han Y. Neuroprotection via inhibition of nitric oxide synthase by bis(7)-tacrine. Neuroreport 2006, 17:471-474.
5. Cristino L., Pica A., Della C.F., Bentivoglio M. Co-induction of nitric oxide synthase, bcl-2 and growth-associated protein-43 in spinal motoneurons during axon regeneration in the lizard tail. Neuroscience 2000, 101:451-458.
6. Thippeswamy T., Haddley K., Corness J.D., Howard M.R., McKay J.S., Beaucourt S.M., Pope M.D., Murphy D., Morris R., Hokfelt T., Quinn J.P. NO-cGMP mediated galanin expression in NGF-deprived or axotomized sensory neurons. J. Neurochem. 2007, 100:790-801.
7. Chu T.H., Wu W.T. Nitric oxide synthase inhibitor attenuates number of regenerating spinal motoneurons in adult rats. Neuroreport 2006, 17:969-973.
8. Gonzalez-Hernandez T., Rustioni A. Nitric oxide synthase and growth-associated protein are coexpressed in primary sensory neurons after peripheral injury. J. Comp. Neurol. 1999, 404:64-74.
9. Fiallos-Estrada C.E., Kummer W., Mayer B., Bravo R., Zimmermann M., Herdegen T. Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci. Lett. 1993, 150:169-173.
10. Zhang X., Verge V., Wiesenfeld-Hallin Z., Ju G., Bredt D., Synder S.H., Hokfelt T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J. Comp. Neurol. 1993, 335:563-575.
11. Rydh-Rinder M., Holmberg K., Elfvin L.G., Wiesenfeld-Hallin Z., Hokfelt T. Effects of peripheral axotomy on neuropeptides and nitric oxide synthase in dorsal root ganglia and spinal cord of the guinea pig: an immunohistochemical study. Brain Res. 1996, 707:180-188.
12. Verge V.M., Xu Z., Xu X.J., Wiesenfeld-Hallin Z., Hokfelt T. Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc. Natl. Acad. Sci. USA 1992, 89:11617-11621.
13. Gonzalez-Hernandez T., Rustioni A. Expression of three forms of nitric oxide synthase in peripheral nerve regeneration. J. Neurosci. Res. 1999, 55:198-207.
14. Allen G.W., Liu J., Kirby M.A., De L.M. Induction and axonal localization of epithelial/epidermal fatty acid-binding protein in retinal ganglion cells are associated with axon development and regeneration. J. Neurosci. Res. 2001, 66:396-405.
15. Benowitz L.I., Perrone-Bizzozero N.I., Finklestein S.P. Molecular properties of the growth-associated protein GAP-43 (B-50). J. Neurochem. 1987, 48:1640-1647.
16. Benowitz L.I., Perrone-Bizzozero N.I., Neve R.L., Rodriguez W. GAP-43 as a marker for structural plasticity in the mature CNS. Prog. Brain Res. 1990, 86:309-320.
17. Benowitz L.I., Goldberg D.E., Irwin N. Inosine stimulates axon growth in vitro, in the adult CNS. Prog. Brain Res. 2002, 137:389-399.
18. Irwin N., Chao S., Goritchenko L., Horiuchi A., Greengard P., Nairn A.C., Benowitz L.I. Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19. Proc. Natl. Acad. Sci. USA 2002, 99:12427-12431.
19. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 2003, 23:2284-2293.
20. Wu W., Li L. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci. Lett. 1993, 153:121-124.
21. Yu W.H. Nitric oxide synthase in motor neurons after axotomy. J. Histochem. Cytochem. 1994, 42:451-457.
22. Wu Y., Li Y., Liu H., Wu W. Induction of nitric oxide synthase and motoneuron death in newborn and early postnatal rats following spinal root avulsion. Neurosci. Lett. 1995, 194:109-112.
23. Gu Y., Spasic Z., Wu W. The effects of remaining axons on motoneuron survival and NOS expression following axotomy in the adult rat. Dev. Neurosci. 1997, 19:255-259.
24. Rossiter J.P., Riopelle R.J., Bisby M.A. Axotomy-induced apoptotic cell death of neonatal rat facial motoneurons: time course analysis and relation to NADPH-diaphorase activity. Exp. Neurol. 1996, 138:33-44.
25. Cristino L., Pica A., Della C.F., Bentivoglio M. Plastic changes and nitric oxide synthase induction in neurons that innervate the regenerated tail of the lizard Gekko gecko: I. Response of spinal motoneurons to tail amputation and regeneration. J. Comp. Neurol. 2000, 417:60-72.
26. Wu W., Liuzzi F.J., Schinco F.P., Depto A.S., Li Y., Mong J.A., Dawson T.M., Snyder S.H. Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 1994, 61:719-726.
27. Wu W. Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: a comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp. Neurol. 1996, 141:190-200.
28. Yuan Q., Hu B., Su H., So K.F., Lin Z., Wu W. GAP-43 expression correlates with spinal motoneuron regeneration following root avulsion. J. Brachial. Plex. Peripher. Nerve Inj. 2009, 4:18.
29. Carlstedt T. Functional recovery after ventral root avulsion and implantation in the spinal cord. Clin. Neurol. Neurosurg. 1993, 95(Suppl.):S109-S111.
30. Carlstedt T., Anand P., Hallin R., Misra P.V., Noren G., Seferlis T. Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J. Neurosurg. 2000, 93:237-247.
31. Gu H.Y., Chai H., Zhang J.Y., Yao Z.B., Zhou L.H., Wong W.M., Bruce I., Wu W.T. Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur. J. Neurosci. 2004, 19:2123-2131.
32. Gu H.Y., Chai H., Zhang J.Y., Yao Z.B., Zhou L.H., Wong W.M., Bruce I.C., Wu W.T. Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp. Neurol. 2005, 192:89-99.
33. Yuan Q., Xie Y., So K.F., Wu W. Inflammatory response associated with axonal injury to spinal motoneurons in newborn rats. Dev. Neurosci. 2003, 25:72-78.
34. Gu H.Y., Chai H., Zhang J.Y., Yao Z.B., Zhou L.H., Wong W.M., Bruce I., Wu W.T. Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur. J. Neurosci. 2004, 19:2123-2131.
35. Wu W., Li L., Yick L.W., Chai H., Xie Y., Yang Y., Prevette D.M., Oppenheim R.W. GDNF and BDNF alter the expression of neuronal NOS, c-Jun, and p75 and prevent motoneuron death following spinal root avulsion in adult rats. J. Neurotrauma 2003, 20:603-612.
36. Verhaagen J., Oestreicher A.B., Gispen W.H., Margolis F.L. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J. Neurosci. 1989, 9:683-691.
37. Kruger L., Bendotti C., Rivolta R., Samanin R. Distribution of GAP-43 mRNA in the adult rat brain. J. Comp. Neurol. 1993, 333:417-434.
38. Oestreicher A.B., De Graan P.N., Gispen W.H., Verhaagen J., Schrama L.H. B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog. Neurobiol. 1997, 53:627-686.
39. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997, 20:84-91.
40. Buffo A., Holtmaat A.J., Savio T., Verbeek J.S., Oberdick J., Oestreicher A.B., Gispen W.H., Verhaagen J., Rossi F., Strata P. Targeted overexpression of the neurite growth-associated protein B-50/GAP-43 in cerebellar Purkinje cells induces sprouting after axotomy but not axon regeneration into growth-permissive transplants. J. Neurosci. 1997, 17:8778-8791.
41. Ikegami T., Nakamura M., Yamane J., Katoh H., Okada S., Iwanami A., Watanabe K., Ishii K., Kato F., Fujita H., Takahashi T., Okano H.J., Toyama Y., Okano H. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur. J. Neurosci. 2005, 22:3036-3046.
42. Zhang Y., Bo X., Schoepfer R., Holtmaat A.J., Verhaagen J., Emson P.C., Lieberman A.R., Anderson P.N. Growth-associated protein GAP-43 and L1 act synergistically to promote regenerative growth of Purkinje cell axons in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:14883-14888.
43. Blits B., Carlstedt T.P., Ruitenberg M.J., de Winter F., Hermens W.T., Dijkhuizen P.A., Claasens J.W., Eggers R., van der S.R., Tenenbaum L., Boer G.J., Verhaagen J. Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adeno-associated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp. Neurol. 2004, 189:303-316.
44. Hoang T.X., Nieto J.H., Tillakaratne N.J., Havton L.A. Autonomic and motor neuron death is progressive and parallel in a lumbosacral ventral root avulsion model of cauda equina injury. J. Comp. Neurol. 2003, 467:477-486.
45. Chong M.S., Woolf C.J., Andrews P., Turmaine M., Schreyer D.J., Anderson P.N. The downregulation of GAP-43 is not responsible for the failure of regeneration in freeze-killed nerve grafts in the rat. Exp. Neurol. 1994, 129:311-320.
46. Coggeshall R.E., Reynolds M.L., Woolf C.J. Distribution of the growth associated protein GAP-43 in the central processes of axotomized primary afferents in the adult rat spinal cord; presence of growth cone-like structures. Neurosci. Lett. 1991, 131:37-41.
47. Verkade P., Oestreicher A.B., Verkleij A.J., Gispen W.H. The increase in B-50/GAP-43 in regenerating rat sciatic nerve occurs predominantly in unmyelinated axon shafts: a quantitative ultrastructural study. J. Comp. Neurol. 1995, 356:433-443.
48. Schreyer D.J., Skene J.H. Injury-associated induction of GAP-43 expression displays axon branch specificity in rat dorsal root ganglion neurons. J. Neurobiol. 1993, 24:959-970.
49. Sommervaille T., Reynolds M.L., Woolf C.J. Time-dependent differences in the increase in GAP-43 expression in dorsal root ganglion cells after peripheral axotomy. Neuroscience 1991, 45:213-220.
50. Wiese U.H., Emson P.C., Sheppard R.C. Production and characterization of an anti-peptide antibody specific for the growth-associated protein, GAP-43. Brain Res. 1991, 554:145-152.